Basic and Applied Herpetology 29 (2015) 109-114

Parasite specificity in bocagei and P. carbonelli () from NW Portugal: a host-parasite history

Vicente Roca*

Departament de Zoologia, Facultat de Ciències Biològiques, Universitat de València, Dr. Moliner 50, 46100 Burjassot, Spain.

* Correspondence: Phone: +34 963544606, Fax: +34 963543049, E-mail: [email protected]

Received: 20 June 2014; returned for review: 4 December 2014; accepted 12 December 2014.

Host parasite specificity is related to several factors including the type of life cycle of the parasite, the occupied by both parasites and hosts, and the food habits of the hosts. In this work, gastrointestinal helminths in two congeneric lacertid , Podarcis bocagei and Podarcis carbonelli living in sintopy, have been analysed. Out of four helminth found, three of them, the trem‐ atode Brachylaima sp., the cestode Oochoristica gallica and the nematode Skrjabinelazia hoffmanni, have indirect life cycles while the nematode Spauligodon carbonelli has a direct life cycle. Heterox‐ enous helminths showed low host specificity whereas S. carbonelli may be placed at an intermediate position in a continuum of the degree of specificity.

Key words: host‐parasite relationships; Iberian Peninsula; lizards; parasites.

Especificidad parasitaria en Podarcis bocagei y P. carbonelli del NO de Portugal: una historia de parásitos y hospedadores. La especificidad parasitaria está relacionada con diversos factores entre los que se incluyen el tipo de ciclo vital del parásito, el hábitat que ocupan parásito y hospe‐ dador, o la estrategia alimentaria de este último. Se analizaron los hospedadores Podarcis bocagei y Podarcis carbonelli (Lacertidae) que habitan un área de sintopía estricta y se estudiaron sus helmintos gas‐ trointestinales. De las cuatro especies de helmintos detectadas, tres de ellas, el trematodo Brachy- laima sp., el cestodo Oochoristica gallica y el nematodo Skrjabinelazia hoffmanni, tienen ciclos vitales indi‐ rectos mientras que el nematodo Spauligodon carbonelli presenta un ciclo directo. Los helmintos de ciclos heteroxenos mostraron una especificidad baja mientras que S. carbonelli ocupa una posición intermedia en un continuo de la especificidad parasitaria.

Key words: lagartijas; parásitos; Península Ibérica; relaciones parásito‐hospedador.

The concept of co‐evolution between extent to which a parasite taxon is restrict‐ parasites and hosts is based on the fact ed in the number of host species used at a that the gradual host‐parasite adaptation given stage in the life cycle (Poulin, 1998). has been adjusting over evolutionary time Highly host‐specific parasites are restrict‐ in mutual gene interaction to get a bal‐ ed to one host species (extreme stenoxeny) anced relationship (Combes, 1995; Mar‐ and specificity declines as the number of tínez‐Fernández Cordero del Campil‐ suitable host species increases (eurixeny) lo, 2007). Host specificity is defined as the (Poulin, 1998). To understand why some

DOI: http://dx.doi.org/10.11160/bah.14005 SHORT NOTES parasites are highly host specific and oth- ber 2001, and January and August 2002. ers are not, it is firstly necessary under- The searched region is a narrow sandy stand how parasites and hosts have co- area consisting in humid covered by evolved since the origin of their associa- psammophilic vegetation, in which both tion (Poulin, loc. cit.). Specificity is related host species are strictly syntopic to diverse conditions, as life cycle of the (Carretero et al., 2002). Lizards were imme- parasite, ecological factors, or physiologi- diately transported to the laboratory, hu- cal characteristics of parasites and hosts, manely sacrificed with an overdose of among others, although its molecular ba- chloroform, and analysed for gastrointesti- ses are still poorly known (Ortega-Mora nal helminths, which were removed, Rojo-Vázquez, 2007). washed, fixed and mounted according to Lacertid lizards Podarcis bocagei standard parasitological techniques (Seoane, 1884) and P. carbonelli Pérez- (GaldÓn, 2007). Helminths were identified Mellado, 1981 are suitable for the study of as accurate as possible according adequate host-parasite specificity because: (i) both bibliography. are considered paraphyletic species (Lima Four helminthic species were found et al., 2008), and (ii) show a peculiar geograph- (Fig. 1), one trematode (Brachylaima sp. ical distribution in Douro littoral region metacercariae), one cestode (Oochoristica galli- (NW Portugal) including a strictly syntop- ca) and two nematodes (Spauligodon carbonelli ic area (Carretero et al., 2002). and Sk rjabinelazia hoffmanni). Three of these In this study I have analysed the gas- species were common to both hosts, and S. trointestinal helminth communities for carbonelli was found in P. bocagei but not in both hosts in order to know the type and P. carbonelli. Table 1 shows their prevalence of degree of specificity of the different hel- infection in each host. minth species found. Although Butcher Grove (2005) sug- Eighty seven specimens of P. bocagei gested that the Australian shingleback liz- and 117 of P. carbonelli were caught by noose ard species (Tiliqua rugosa) may be a defini- and by hand in Espinho and Granja (UTM tive hosts for Brachylaima cribbi, the pres- 10 x 10 km squares, 29T NF24 and NF34). ence of metacercariae (larval forms) of Captures were made in April and Septem- Brachylaima sp. in both Iberian hosts in study may be considered as accidental parasit- Table 1: Prevalence of infection of the hel- ism. This is considered when a parasite minths found in each host. reaches a wrong host in which it is unable Helminth species P. bocagei P. carbonelli to complete its development. As (N = 87) (N = 117) are usually not definitive hosts for these Brachylaima sp. 1.2% 1.7% trematodes, the presence of metacercariae Oochoristica gallica 6.9% 2.6% of Brachylaima spp. in some Iberian liz- ards (see Roca Hornero, 1994) is proba- Spauligodon carbonelli 1.2% - bly due to the ingestion of some terrestrial

Skrjabinelazia hoffmanni 6.9% 4.3% snails, which are second intermediate hosts (González-Moreno, 2002).

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Figure 1: Parasites found in Podarcis lizards. (a) Brachylaima sp. metacercariae from P. bo- cagei. (b) Oochoristica gallica from P. carbonelli, mature proglotids. (c) Spauligodon carbonelli from P. carbonelli: ♂ caudal end of body, ventral view. (d) Skrjabinelazia hoffmanni from P. bocagei: ♂ cau- dal end ventro-lateral view.

The nematode S. hoffmanni is a generalist ca from the Iberian Peninsula (García-Adell species (sensu Edwards Bush, 1989) that Roca, 1988; Roca et al., 1989; GaldÓn et has been recorded in some genera of Pal- al., 2006), it may be considered a Podarcis spe- aearctic lacertid lizards, as Podarcis, cialist. Skrjabinelazia hoffmanni and O. galli- Darevskia and Lacerta (García-Adell Ro- ca would be close to the end of the low specifici- ca, 1988; Roca et al., 1989, 1990; Roca ty (eurixeny) and far from the end of the Hornero, 1994; Biserkov Kostadinova, high specificity (estenoxeny), in a continu- 1998; Yildirimham et al., 2011; V. Roca et um of the degree of specificity, whereas S. al., unpublished data). Also the cestode O. gal- carbonelli would be located at an intermediate lica is a generalist helminth species since it has position between the two extremes (see been recorded in some lizards of the gene- references above). ra Podarcis, Psammodromus and Iberolacerta Brachylaima sp., O. gallica and S. hoffman- (García-Adell, 1987; García-Adell Ro- ni have indirect life cycles, and S. carbonelli ca, 1988; Roca et al., 1989; Roca has a direct life cycle. Probably, O. gallica Hornero, 1994). As the nematode S. car- has a diheteroxenic life cycle in which bonelli has been only recorded in the lizards some terrestrial is involved as Podarcis muralis, P. carbonelli and P. hispani- intermediate host (some coleopteran in-

111 SHORT NOTES sects and crustacean isopods have been studied, the chances of contact with the recorded in the case of other species be- infective eggs of S. carbonelli are the same for longing to the genus Oochoristica, García- both lizards. Therefore, are ethological Adell, 1987). In the case of species of the conditions determining the presence of the genus Skrjabinelazia, Chabaud et al. (1988) parasite in a host but not in the other? Ro- and Roca et al. (1990) also pointed out a di- ca et al. (2006) pointed out that both host spe- heteroxenic life cycle in which a coproph- cies are parasitized by S. carbonelli in other agous would be the intermediate areas of NW Portugal and suggested that host. As larval forms of Sk rjabinelazia spp. variation in the prevalence of infection of do not suffer any change in those , both hosts is due to local environmental they should be considered paratenic hosts conditions rather than to ethological (Chabaud et al., 1988). differences between the two species, or to Since heteroxenic helminths infect both host specificity. However, this does not hosts, it seems that the area inhabited by explain the absence of this nematode in P. the studied lizards is suitable for arthro- carbonelli in the syntopic area. pods and gastropods which are intermedi- Is it relevant to consider a type of phy- ate hosts. Ecological factors favour the en- logenetic specificity that implies the union counter and facilitates the flow of the life over prolonged periods of host-parasite cycle of those parasites and so they show interspecific contact, in the course of their an ecological host specificity (Ortega- evolution? It does not seem appropriate to Mora Rojo-Vázquez, 2007). Since both refer to host specificity sensu stricto since S. hosts show similar eating behaviour (strict carbonelli has been recorded in several Po- carnivores, Roca et al., 2006), an ethological darcis species in the Iberian Peninsula. How- specificity should also be considered ever, it is noteworthy the absence of this (Ortega-Mora & Rojo-Vázquez, loc. cit.). nematode in the endemic lacertid lizards These two types of specificity do not need of the Balearic archipelago, Podarcis a long contact time in the evolution of both pityusensis and P. lilfordi, in which S. car- parasite and host, and so they fall close to bonelli is apparently replaced by the congeneric the extreme of eurixeny in a continuum of S. cabrerae (Roca Hornero, 1994). It the degree of specificity. should be considered the possibility of a The more interesting helminth species common ancestor of both species of regarding the relationships with their Spauligodon and a speciation of this genus hosts is S. carbonelli. Its life cycle is direct, parallel to the speciation of the ancestor which means that the host lizards are in- that resulted in the current Balearic Po- fested through accidental ingestion of eggs darcis (Alcover, 1988). From this point of that are associated with the substrate or view, it is pertinent to consider a presuma- adhered to the cloaca region of their hosts ble phylogenetic relationship of the nema- (Roca et al., 2006). So, why is the parasite todes S. carbonelli and S. cabrerae regarding present in P. bocagei but not in P. carbonelli? the phylogenetic relationship of hosts of Related to the biotic and abiotic conditions Podarcis group in the Iberian Peninsula and in the area of sintopy where the hosts were the Balearic Islands.

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Jorge et al. (2011) used molecular meth- Carretero, M.A.; Sa Sousa, P.; Barbosa, D.; ods to show that the different species of Harris, D.J. Pinho, C. (2002). Sintopía lizards of the genus Gallotia in the Canary estricta entre Podarcis bocagei y P. carbonelli. Islands were colonized by two independ- Boletín de la Asociación Herpetológica Española 13: 20-24. ent Spauligod on lineages. This led to the Combes, C. (1995). Interactions Durables. Écolo- description of two different species of this gie et Évolution du Parasitisme. Masson, Paris, genus, S. atlanticus from the islands of Lanza- France. rote and Fuerteventura and S. occidentalis Chabaud, A.G.; Bain, O. Poinar, G.O., Jr. from the western islands (Jorge et al., (1988). Skrjabinelazia galliardi (Nematoda: 2013). Thus, it would be appropriate in Seuratoidea): compléments morpholo- this kind of studies to concretize the phy- giques et cycle biologique. Annales de Para- logenetic relationships and the possible co- sitologie Humaine et Comparée 63: 278-284. evolution between Ibero-Balearic nema- Edwards, D.D. Bush, A.O. (1989). Helminth communities in avocets: Importance of todes of the genus Spauligodon and hosts compound community. Journal of Parasitol- of Podarcis group. ogy 98: 439-445. GaldÓn, M.A. (2007). Estudio Parasitológico de Acknowledgement Podarcis bocagei y Podarcis carbonelli (Sauria: Lacertidae) del Noroeste de Portugal. This study was partially funded by the Tesis Doctoral, Universitat de València, projects POCTI/BSE/45664/2002 and OCI/ Burjassot, Spain. BIA-BDE/55865/2004 of Fundação para a GaldÓn, M.A.; Roca, V.; Barbosa, D. Carre- Ciência e a Tecnologia, FCT (Portugal). tero, M.A. (2006). Intestinal helminth com- Collecting permits were provided by Insti- munities of Podarcis bocagei and Podarcis tuto de Conservação da Natureza, ICN carbonelli (Sauria: Lacertidae) in NW Portugal. (Portugal). Thanks to B. Fráguas, D.J. Har- Helminthologia 43: 37-41. ris, R. Pereira, C. Soares and P. Sousa for García-Adell, G. (1987). Helmintofauna de help with fieldwork. An anonymous refer- Algunas Especies de Reptiles de los Pirineos Ibéricos. Tesis de Licenciatura, Universitat de ee helped to improve the English language València, Burjassot, Spain. and the quality of the manuscript. García-Adell, G. Roca, V. (1988). Helminto- fauna de lacértidos de los Pirineos centrales References ibéricos. Revista Ibérica de Parasitología 48:257-267. Alcover, J.A. (1988). Las faunas preneolíticas González-Moreno, O. (2002). Brachylaima. de las islas mediterráneas. Mundo Científico Contribución al Conocimiento de la Bionomía de 80: 504-517. Digénidos de la Familia Brachylaimidae Joyeux Biserkov, V. Kostadinova, A. (1998). Intesti- et Foley, 1930, en el Delta del Llobregat. Tesis nal helminth communities in the green li- Doctoral, Universitat de Barcelona, Barcelo- zard Lacerta viridis from Bulgaria. Journal of na, Spain. Helminthology 72: 267-271. Jorge, F.; Roca, V.; Perera, A.; Harris, D.J. Butcher, A.R. Grove, D.I. (2005). Second in- Carretero, M.A. (2011). A phylogenetic termediate host land snails and definitive assessment of the colonisation patterns in host of Brachylaima cribbi in Spauligodon atlanticus Astasio-Arbiza et al., Southern Australia. Parasite 12: 31-37. 1987 (Nematoda: Oxyurida: Pharyngodoni-

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